Imaging Science in Dentistry 2021; 51: 209-16 https://doi.org/10.5624/isd.20200313

Three-dimensional cone-beam computed tomographic sialography in the diagnosis and management of primary Sjögren syndrome: Report of 3 cases

Nithin Thomas 1, Aninditya Kaur 2, Sujatha S. Reddy 3, Rakesh Nagaraju 3,*, Ravleen Nagi 4, Vidya Gurram Shankar 5 1Department of Oral Radiology, Maxillofacial Diagnostics, Cochin, India 2Department of Oral Radiology, DMD Imaging, Gurgaon, India 3Department of Oral Medicine and Radiology, Faculty of Dental Sciences, M.S. Ramaiah University of Applied Sciences, Bangalore, Karnataka, India 4Department of Oral Medicine and Radiology, Swami Devi Dyal Hospital and Dental College, Panchkula, Haryana, India 5Department of Public Health, Texila American University, Georgetown, Guyana

ABSTRACT

Sjögren syndrome is a chronic autoimmune inflammatory disease characterized by lymphocytic infiltration of exocrine glands, predominantly the parotid and lacrimal glands, thereby resulting in oral and ocular dryness. It has been reported to occur most frequently in women between 40 and 50 years of age. Sjögren syndrome has an insidious onset, is slowly progressive, and presents a wide range of clinical manifestations, leading to delays or challenges in the diagnosis. Early diagnosis of this condition is essential to prevent the associated complications that affect patients’ quality of life. This report presents 3 cases of Sjögren syndrome in female patients aged between 40 and 75 years who presented with complaints of persistent dry mouth and burning sensation. The cases highlight the diagnostic value of 3-dimensional cone-beam computed tomographic sialography in the detection of salivary gland pathologies at an early stage. (Imaging Sci Dent 2021; 51: 209-16)

KEY WORDS: ‌Cone-Beam Computed Tomography; Diagnosis; Sialography; Sjögren Syndrome; Xerostomia

Sjögren syndrome is a chronic autoimmune disease cha­ of Sjögren syndrome, as demonstrated by the presence of racterized by immunologically mediated destruction of autoreactive T and B lymphocytes, abnormal regulation of exocrine glands, mainly the salivary and lacrimal glands. apoptosis, production of autoantibodies to ribonucleopro­ This condition results in dry mouth (xerostomia) and dry tein particles (anti-SSA/Ro and anti-SSB/La), and lympho­ eyes (keratoconjunctivitis sicca). Its primary form involves cytic infiltration of glandular tissues; these processes event­-­ exocrine glands, while its secondary form is associated with ually interfere with glandular function and result in impaired­ other autoimmune disorders.1 The prevalence of Sjögren secretory activity, particularly of the salivary and lacrimal­ syndrome in the general population has been estimated to be glands.3 0.5% to 4.8%, it commonly occurs in middle-aged women Sjögren syndrome has variable clinical presentations, between 40 and 50 years of age, and its male-to-female ratio ranging­ from local exocrinopathy to the involvement of has been reported to be 1 : 9.2 The etiopathogenesis of this multiple­ organs, and affected individuals have an increased syndrome remains elusive, but the adaptive immune system risk of B cell non-Hodgkin lymphoma. Studies have repor­ has been documented to play an important role in the onset ted the presence of autoantibodies to ribonucleoprotein particles (anti-SSA/Ro and anti-SSB/La) in the majority of Received November 20, 2020; Revised January 16, 2021; Accepted January 18, 2021 Sjögren syndrome patients. The diagnosis is often delayed *Correspondence to : Prof. Rakesh Nagaraju Department of Oral Medicine and Radiology, Faculty of Dental Sciences, M.S. for years in many patients because the clinical symptoms of Ramaiah University of Applied Sciences, New BEL Road, MSRIT Post, MSR Nagar, Sjögren syndrome mimic those of other medical conditions Bangalore, Karnataka, 560054, India Tel) 91-9448507494, E-mail) [email protected] such as xerostomia due to diabetes mellitus, psychotropic

Copyright ⓒ 2021 by Korean Academy of Oral and Maxillofacial Radiology This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Imaging Science in Dentistry·pISSN 2233-7822 eISSN 2233-7830

- 209 - Three-dimensional cone-beam computed tomographic sialography in the diagnosis and management of primary Sjögren syndrome... drugs, sialadenosis, and viral infections.3 The diagnosis be­ mild dryness, 4-6 moderate dryness and 7-10 severe dry­ comes even more challenging for the clinician if the patient ness, as depicted in Table 3. presents with persistent symptoms and without any detec­ Various imaging techniques such as conventional radio­ table bilateral parotid gland swelling; therefore, it is essential­ graphy, computed tomography (CT), cone-beam CT (CBCT), to establish a proper diagnosis at an early stage to prevent sialoendoscopy, ultrasonography, and magnetic resonance complications and to achieve better treatment outcomes. (MR) imaging are used to complement the diagnosis of Numerous standards have been proposed for the diag­nosis Sjögren syndrome. Sialography, which is one of the most of Sjögren syndrome, of which the most widely accep- widely used techniques, enhances visualization of the ductal ­ted is the American and European Group (AECG) criteria, architecture and gland parenchyma following an injection of according to which the diagnosis should be based on 6 para­ radiopaque contrast media.5 One of the typical sialographic meters: 1) the presence of ocular symptoms; 2) oral symp­ appearances of Sjögren syndrome, as described by Rubin and toms of hyposalivation, 3) positive ocular signs assessed by Holt, is “sialodochiectasis or sialectasis,” which can mani­ the Schirmer and Rose Bengal dye test; 4) biopsies of minor fest as punctate, globular, cavitary, and destructive patterns salivary glands and/or lacrimal glands; 5) abnormal oral on sialograms.6 Three-dimensional (3D) CT, CBCT, and signs such as unstimulated whole salivary flow (<1.5 mL in MR sialography are recently introduced imaging modalities 15 minutes), abnormal parotid sialography and salivary that provide 3D images of the salivary gland ductal archi­ scinti­ ­graphy findings; and 6) assays for anti-SSA/Ro or anti- tecture, unlike other modalities.7 This paper emphasizes the SSB/La antibodies (Table 1).4-9 For a definitive diagnosis of diagnostic value of 3D CBCT sialography in 3 cases of pri­ primary Sjögren syndrome, at least 4 of the 6 criteria should mary Sjögren syndrome. be met, including positive results for the minor salivary gland 4 biopsy or antibody test. In addition, the severity of oral Case Report dryness can be quantified by the Xerostomia Inventory and Case 1 Challacombe scales of clinical oral dryness.9 The Xerosto­ A 44-year-old female patient was referred to Depart­ mia Inventory scale consists of 11 items, each on a 5-point ment of Oral Medicine and Radiology due to a complaint Likert scale (Table 2), whereas the Challacombe scale is a of dry mouth and recurrent episodes of swelling in the left 10-point scale in which an additive score of 1-3 indicates parotid region for 5 years. She also complained of multi­ ple decayed teeth. Her past dental history revealed that she Table 1. Revised American-European Consensus Criteria for Sjög­ ren syndrome4 had visited many private clinics and otolaryngologists for the same problem, for which only medications were given.

1) Ocular symptoms (at least one present) The patient’s medical, family, and drug history were non- Symptoms of dry eyes for at least 3 months remarkable. On an extraoral examination, no abnormality A foreign body sensation in the eyes Use of artificial tears 3 or more times per day was seen, and the right and left parotid glands were normal

in shape and size. An intraoral examination showed signs of 2) Oral symptoms (at least one present) Symptoms of dry mouth for at least 3 months Recurrent or persistently swollen salivary glands Table 2. The series of questions assessed by the Xerostomia Inven­ Need for liquids to swallow dry foods tory subjective scale for oral dryness8

3) Objective ocular signs (at least one present) - I sip liquids to aid in swallowing food.

Abnormal Schirmer’s test - My mouth feels dry when eating a meal. (without anaesthesia; ≤5 mm/5 minutes) - I get up at night to drink. Positive vital dye staining of the eye surface - My mouth feels dry. 4) Histopathology - I have difficulty in eating dry foods.

Lip biopsy showing focal lymphocytic sialoadenitis - I suck sweets or cough lollies to relieve dry mouth. (focus score ≥1 per 4 mm2) - I have difficulties swallowing certain foods.

5) Oral signs (at least one present) - The skin of my face feels dry.

Unstimulated whole salivary flow (≤1.5 mL in 15 minutes) - My eyes feel dry. Abnormal parotid sialography Abnormal salivary scintigraphy - My lips feel dry. - The inside of my nose feels dry. 6) Autoantibodies (at least one present) Anti-SSA (Ro) or Anti-SSB (La), or both Response options: 1: never, 2: hardly, 3: occasionally, 4: fairly often, 5: very often.

- 210 - Nithin Thomas et al dryness of the oral mucosa, with the mouth mirror sticking of Oral Medicine and Radiology with a chief complaint of to the right and left buccal mucosa and dorsum of the dry mouth and burning sensation in the mouth while con­ tongue. Cervical caries of the upper and lower anterior teeth, suming hot and spicy foods. She was initially diagnosed as well as mild depapillation of the dorsum of the tongue, with oral candidiasis at our department, but her complaint were observed (Fig. 1). Additive scores of 51 in the Xero­ of dryness persisted even after treatment with antifungal stomia Inventory scale8 and 4 in the Challacombe scale of therapy. The patient had a known history of diabetes and clinical oral dryness9 were suggestive of moderate dryness hypertension in the past 8 years and was taking medication. of the oral mucosa. Milking of the bilateral parotid glands Extraorally, no abnormality was seen, the right and left paro- revealed reduced salivary flow through the ducts (Tables 2 tid glands were normal in shape and size. On an intraoral and 3). examination, there was dryness of the oral mucosa, with the mouth mirror sticking to the right and left buccal mucosa Case 2 and dorsum of the tongue. Cervical caries of the upper and A 65-year-old female patient was referred to the Depart­ lower anterior teeth, no pooling of saliva in the floor of the ment of Oral Medicine and Radiology for a complaint of mouth, severe depapillation and lobulations of the dorsum of dry mouth and recurrent episodes of swelling and pain in the tongue, and altered gingival architecture were observed.­ the right and left parotid regions for the last 6 years. She Additive scores of 54 in the Xerostomia Inventory scale had visited many otolaryngologists for the same complaint, and 7 in the Challacombe scale of clinical oral dryness were and antibiotics and analgesics for swelling and pain were suggestive of severe dryness of the oral mucosa. Milking of given. No further investigations or treatment was done. The the bilateral parotid glands revealed severely reduced sali­ patient’s medical, family, and drug history were non-con­ vary flow through the ducts (Tables 2 and 3). tributory. On an extraoral examination, no abnormality was detected; the right and left parotid glands were normal in Investigations shape and size. An intraoral examination showed dryness of Conventional plain film radiography did not demonstrate the oral mucosa, with the mouth mirror sticking to the right any significant findings; therefore, all 3 patients underwent and left buccal mucosa and dorsum of the tongue. Cervical 3D CBCT sialography. Informed consent was obtained caries of the upper and lower anterior teeth, no pooling of from the patients after explaining the procedure. Thereafter, saliva in the floor of the mouth, and mild depapillation of the the parotid duct orifice of the right and left parotid glands dorsum of the tongue were observed. Additive scores of 38 for each patient were located, scout views were obtained, in the Xerostomia Inventory scale and 5 in the Challacombe and 4 mL of iodinated contrast medium (iohexol; Omnipa­ scale of clinical oral dryness were suggestive of moderate que-350, Shanghai, China) was injected into the efferent dryness of the oral mucosa. Milking of the bilateral parotid parotid duct bilaterally under aseptic conditions using a lac­ glands revealed reduced salivary flow through the ducts rimal cannula until the patient felt fullness. Image acqui­sition (Tables 2 and 3). was performed by CBCT (Carestream CS9300 Premium, Carestream Health, Rochester, NY, USA), using the follow­ Case 3 ing operational parameters: 17×13.5 cm field of view, 70 A 75-year-old female patient presented to the Department kVp tube voltage, a tube current of 6.3 mA, and an exposure

Table 3. Challacombe scale of clinical oral dryness9

Additive score Clinical signs Treatment

1-3, Mirror sticks to buccal mucosa, May not need treatment. Mild dryness tongue and frothy saliva Sugar-free chewing gum for 15 minutes twice daily, hydration and routine check-up monitoring required 4-6, No saliva pooling in floor of mouth, Sugar-free chewing gum or sialagogues, Moderate dryness tongue shows mild depapillation, and saliva substitutes and topical fluorides, altered gingival architecture and monitoring at regular intervals 7-10, Glassy appearance of oral mucosa, Saliva substitutes and topical fluorides, Severe dryness tongue fissured/lobulated, cervical caries cause of hyposalivation needs to be ascertained in more than two teeth, and and monitoring at regular intervals debris on palate or sticking to teeth

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A

B

C

Fig. 1. Three-dimensional cone-beam computed tomography sialographic images of 3 cases depict the multiple globular type of sialectasis within the glandular architecture giving a characteristic “cherry blossom” radiographic appearance of both the right and left parotid glands. Preoperative, filling, and emptying phase times for case 1: 2 minutes, 4 minutes and ≥2 hours, respectively (A), case 2: 3 minutes, 4 min­ utes and ≥2 hours (B), and case 3: 3 minutes, 5 minutes and ≥2 hours (C).

- 212 - Nithin Thomas et al time adjusted based on scout views. The data acquisition nuclear antibodies (ANA) produced a speckled pattern on an time for the scan was 9.0 seconds. Images were analysed on a indirect immunofluorescence assay. Based on the above 19-inch liquid crystal display with a resolution of 1,280× investigatory findings, the absence of extraglandular symp­ 1,024 pixels (Dell, Round Rock, TX, USA) at the Department toms, and the presence of 5 of the 6 AECG criteria,4 the final of Radiology, Faculty of Dental Sciences, Ramaiah Uni­ diagnosis of primary Sjögren syndrome was given. versity of Applied Sciences, Bangalore, India. Images were adjusted for contrast and brightness by software tools and Treatment plan reconstructed into 3D images. The multiple globular type of Patients were advised to take small sips of water while sialectasis within the glandular architecture, giving a “cherry eating dry food, avoid speaking continuously, to chew or blossom” radiographic appearance characteristic of Sjögren suck on sugar-free gum, candies, or lemon slices to stimulate syndrome, was observed (Fig. 1). Table 4 shows the time salivation, and to use artificial tear substitutes. Continuous taken for the 3 phases of sialography (preoperative filling, milking of the glands was done through external pressure filling, and emptying). Based on the 3D sialographic find­ to ensure that any blockage present within the ducts was ings, the working diagnosis of primary Sjögren syndrome removed. One patient, aged 75 years, was advised to consult was made. with her physician to check whether the antihypertensive and Further investigations were performed to confirm the antidiabetic medications she was taking may have been the diagnosis of primary Sjögren syndrome. In a quantitative cause of oral dryness. Intraglandular saline lavage of right assessment of the salivary flow rate, unstimulated whole and left parotid glands was done for each patient by inject­ salivary flow rate was found to be <1.5 mL/15 minutes, ing isotonic saline within the glands, which helps to flush suggestive of reduced saliva production as per the AECG the glands by removing any mucous plugs within the ducts criteria (Table 1). The patients were positive for the Schirmer and prevents the formation of sialoliths. This procedure was test, indicating insufficient tear production bilaterally (Table done for the bilateral parotid glands of each patient every 4). The anti-SSA/Ro autoantibody test was positive and anti- day for 4 weeks.

Table 4. Three-dimensional cone-beam computed tomography (CBCT) sialography and Schirmer test findings

Case 1 Case 2 Case 3

Phases of CBCT sialography Preoperative phase (minutes) 2 3 3 Filling phase (minutes) 4 4 5 Emptying phase (hours) ≥2 ≥2 ≥2 Schirmer test results <10/5 minutes (positive) <15/5 minutes (positive) <10/5 minutes (positive)

A B C

Fig. 2. After 4 months, computational dynamic images taken with 3D Slicer open software version 4.10.2 show the dye evacuation time at 0 (blue color; A), 30 (green color; B), and 60 minutes (yellow color; C), respectively, after 3D CBCT sialography, suggestive of improved functional activity of the parotid glands.

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Table 5. Follow-up (at 4 months post-treatment) scores of the Xerostomia Inventory and Challacombe scales

Case 1 Case 2 Case 3 Scale Before After Before After Before After

Xerostomia Inventory (subjective) 51 30 38 14 53 42 Challacombe scale (objective) 4 2 5 2 7 4

Each of our patients also underwent transcutaneous elec­ since been considered the gold standard for demonstrating trical nerve stimulation (TENS), involving the application fine gland ductal structures. Moreover, functional assess­ of adhesive electrode pads over the right and left parotid ment of salivary glands is possible by observing the rate of region for 15 minutes every day for 4 weeks. Patients were excretion of contrast medium from the ducts.12, 13 Plain ima­ followed up for 4 months every 15 days to assess their ging has been extensively used with sialography to identify treatment­ response. After 4 months, milking of the bilateral ductal inflammatory and degenerative diseases, including parotid glands of each patient showed improvements in the sialoliths, sialectasis, fistulae, ductal strictures, and tumours. salivary­ flow rate. Computational dynamic images taken Sialectasis is a typical radiographic appearance of both with 3D Slicer open software version 4.10.2 (http://www. Sjögren syndrome and sialadenitis, and manifests as dots slicer.org) revealed that the dye evacuation time had dec­ and blobs of contrast agent within the gland on sialograms. reased to 1 hour, from 2 hours at the initial visit, suggestive It is characterized by a patent, non-dilated main duct with of improved functional activity of the parotid glands after uniform punctate or globular collections of contrast medium 3D CBCT sialography (Fig. 2 and Table 5). throughout the gland, which represent the extravasation of contrast medium outside the duct lumen through weakened duct walls. Although multiple globular sialectasia could lead Discussion to the diagnosis of primary Sjögren syndrome, this condi­ Sjögren syndrome is a slowly progressive chronic auto­ tion should be differentiated from chronic parotid sialadeni­ immune disorder characterized by symptoms of dry mouth tis. The underlying disease process allowing the collection and eyes, referred to as “sicca symptoms.”1, 2 In some cases, of contrast medium in form of dots or blobs is different; recurrent swelling in the parotid gland leads patients to in Sjögren syndrome, the epithelium lining the intercalated consult multiple specialists without any symptomatic relief; ductule becomes weakened, whereas in sialadenitis, the furthermore, diagnosing the underlying cause of xerostomia acinus becomes dilated and eventually results in extravasa­ that persists for >3 months is a challenge for dental profes­ tion of contrast medium out of the duct.1, 2 The sialographic sionals.10, 11 Early diagnosis is mandatory to achieve better staging of sialectasia seen in Sjögren syndrome is based on clinical outcomes and prevent the complications associated the criteria of Rubin and Holt,6 which divide it into 5 cate­ with Sjögren syndrome. Unfortunately, reaching a diagnosis gories: normal, punctate (smooth oval ≤1 mm), globular can often be difficult and has been reported to take an aver­ (smooth oval 1-2 mm), cavitary (smooth oval >2 mm) and age of 3 years from the onset of symptoms. It is well esta­ destructive­ (irregular >2 mm). Cavitary and destructive sia­ blished that no single investigation can rule out Sjögren syn­ lectasis are more prevalent in advanced cases, and punctate drome. Most often, this condition is diagnosed by rheumato­ foci of calcifications in major salivary glands and multiple logists and immunologists at a later stage by using an expen­- cystic or solid intraglandular masses in a miliary pattern are sive diagnostic test. In our cases, anti-SSA/Ro autoantibody occasionally seen in Sjögren syndrome patients.14 was found to be positive and ANA produced a typical “spe­ However, two-dimensional (2D) images offer low con­ ck­led pattern” on an indirect immunofluorescence assay; trast resolution, therefore, sialography has been combined these findings play an important role in the differentiation of with CT, but CT has the disadvantage of a high radiation sicca symptoms due to other causes than autoimmune dis­ dose and anisotropic voxel resolution obscures the fine ana­ eases. In addition to clinical examinations, we established tomy of ductal structures.5 Moreover, as Sjögren syndrome the working diagnosis of primary SS at an early stage by progresses, fatty degeneration or cystic changes indicative performing 3D CBCT sialography. of destruction of gland in advanced stages are not well app­ Sialography was first mentioned by Carpy in 1902 has reciable on 2D images. As a recently introduced technique,

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MR sialography has been shown to have higher sensitivity swelling. The high diagnostic accuracy is attributed to the and specificity than conventional sialography in demon­ isotropic voxel resolution offered by CBCT in comparison strating non-calcified sialoliths and globular sialectasis as­ to other imaging modalities.2 sociated with chronic sialadenitis and Sjögren syndrome.5 Three-dimensional CBCT sialographic images could assist In addition, MR sialography is non-invasive and could the clinician in the formulation of a proper treatment plan be performed in acutely inflamed glands in which CT im­ and in timely initiation of therapeutic intervention. Symp­ ages fail to reveal any relevant findings. High signal foci tomatic treatment forms the mainstay of the management measuring between 1-2 mm or >2 mm on T2-weighted of Sjögren syndrome. Izumi et al. evaluated the efficacy of MR images in comparison to the surrounding muscle are corticosteroid and saline lavage of parotid glands in relie­ving suggestive of Sjögren syndrome, but the high cost of MR xerostomia in patients with Sjögren syndrome and found imaging restricts its routine clinical application. 3D CBCT that salivary flow significantly improved.18 Studies have sialography is becoming popular over conventional sialo- also reported using TENS for the symptomatic improve­ graphy as it is non-invasive, reliable and provides 3D images ment of xerostomia in patients with radiotherapy.19, 20 In of the ductal system and intraglandular structures with high 2015, Aggarwal et al.19 showed that TENS significantly im­ spatial resolution.14 In our patients, 3D sialograms revealed proved the whole salivary flow rate with little or minimal multiple areas of globular sialectasia with a “cherry blossom side effects. In the present study, all the patients were treated appearance” or “branchless fruit laden tree,” highly sugges­ with saline lavage and TENS for a period of 4 weeks. The tive of Sjögren syndrome, and the procedure was well tol­ patients were followed up for 4 months every 15 days and erated by the patients. Moreover, due to high resolution of were found to have reduced subjective and objective oral CBCT sialography, the image is not affected by metallic res­ symptoms as estimated by the Xerostomia Inventory and toration; this technique enables more accurate mapping of Challacombe scale, as well as improved glandular function salivary gland ducts to detect sites of stenosis, dilatation, and as assessed through 3D CBCT sialography. the presence of salivary stones than is possible with CBCT To conclude, oral physicians play a prime role in identi­ alone. fying and managing Sjögren syndrome with a multifactorial To our best knowledge, this is the first attempt to evaluate etiology. Many Sjögren syndrome patients go undiagnosed the diagnostic performance of 3D CBCT sialography in or are left untreated and seek multiple consultations due to Sjögren syndrome patients. The literature contains a paucity the overlapping symptoms of oral and ocular dryness with of studies emphasizing the diagnostic capability of CBCT other conditions. Proper diagnosis of Sjögren syndrome at sialography in the detection of sialodochitis or ductal sialad­ an early stage can greatly improve patients’ quality of life. enitis, sialoliths, and abnormal glands with chronic inflam­ Three-dimensional sialography has been found to be a pro­ matory changes. Bertin et al.15 examined 27 patients with mising noninvasive imaging modality for detecting salivary parotid and submandibular salivary symptoms using 3D gland pathologies in peripheral ducts that provides clinicians CBCT sialography and suggested that this technique ena­ with high-quality 3D images of the intraglandular ductal sys­ bled a precise analysis of the ductal system in cases of non- tem. Future case studies should be conducted to validate the tumorous chronic inflammatory salivary gland pathologies. diagnostic accuracy of this method in patients with salivary The main lesions found were lithiasis and mucous plugs gland diseases. in 29.6% of patients, evidenced by duct filling defects and chronic salivary injuries that presented a “dead tree app­ Conflicts of Interest: None earance” in 25.9% of patients. 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